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Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 DOI 10.1186/s12862-017-1076-y

RESEARCH ARTICLE Open Access Re-evaluation of the Haarlem and the radiation of maniraptoran theropod Christian Foth1,3 and Oliver W. M. Rauhut2*

Abstract Background: Archaeopteryx is an iconic that has long been pivotal for our understanding of the origin of . Remains of this important have only been found in the Late lithographic of Bavaria, Germany. Twelve skeletal specimens are reported so far. Archaeopteryx was long the only pre- paravian theropod known, but recent discoveries from the , , yielded a remarkable diversity of this , including the possibly oldest and most basal known clade of avialan, here named Anchiornithidae. However, Archaeopteryx remains the only Jurassic paravian theropod based on diagnostic material reported outside China. Results: Re-examination of the incomplete Haarlem Archaeopteryx specimen did not find any diagnostic features of this . In contrast, the specimen markedly differs in proportions from other Archaeopteryx specimens and shares two distinct characters with anchiornithids. Phylogenetic analysis confirms it as the first anchiornithid recorded outside the Tiaojushan Formation of China, for which the new generic name Ostromia is proposed here. Conclusions: In combination with a biogeographic analysis of coelurosaurian theropods and palaeogeographic and stratigraphic data, our results indicate an explosive radiation of maniraptoran coelurosaurs probably in isolation in eastern Asia in the late and a rapid, at least Laurasian dispersal of the different subclades in the . Small body size and, possibly, a multiple origin of capabilities enhanced dispersal capabilities of paravian theropods and might thus have been crucial for their evolutionary success. Keywords: , Anchiornithidae, Late Jurassic, Biogeography, Radiation

Background Recent discoveries in the probably Tiaojishan Having been discovered only 2 after Darwin’s[1] Formation [6, 7] of eastern China have changed this pic- prediction that intermediate forms of different ture. In the past 15 years, numerous taxa of maniraptoran should be present in the fossil record, the famous ‘Urvogel‘ coelurosaurs were found in this formation. Although the Archaeopteryx from the limestones of southern phylogenetic relationships of these taxa are still disputed Germany [2] has not only played an important role in [4, 5, 8, 9], at least the genera and the initial discussion of Darwin’s theory [3], but became are usually considered to form a monophyletic, endemic the ‘yard-stick’ for – the taxon to which clade [4, 8–10], which were recently considered to be the any new relevant discovery is compared [4, 5]. How- oldest known avialans [9]. Indeed, with the exception of ever, Archaeopteryx remainedtheonlyJurassicparavian some fragmentary and questionable remains (mainly theropod known from diagnostic material for more than isolated teeth), no paravian theropod but Archaeopteryx 100 years. has so far been reported from Jurassic rocks outside China. Although the discovery of the first Archaeopteryx

* Correspondence: [email protected] was announced by von Meyer [2], a fragmentary paravian 2SNSB-Bayerische Staatssammlung für Paläontologie und Geologie, theropod was found 6 years earlier, but misidentified as a Ludwig-Maximilians-University Munich, Department for Earth and new of the Pterodactylus, P. crassipes [11]. Environmental Sciences, and GeoBioCenter, Richard-Wagner-Str. 10, 80333 Munich, Germany It was not until 1970 that this specimen (Fig. 1) was Full list of author information is available at the end of the article correctly identified as theropod and referred to the genus

© The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 2 of 16

which is most probably the reason why this specimen has not been included in previous evaluations of the pro- portions of Archaeopteryx [14, 15]. Ostrom [16] and Wellnhofer [13] provided measurements for this speci- men, but noted that most of them where either incomplete, or based on estimations. In order to compare the Haarlem specimen to other Archaeopteryx specimens, we thus took new measurements from a high quality cast held at the Bayerische Staatssammlung für Paläontologie und Geologie (SNSB-BSPG 1971 I 211), and verified anatomical fea- tures by personal observations of the original specimen (Teylers Museum TM 6928, 6929), which was examined in July 2016. Only elements that could be measured directly or estimated with high certainty were considered here (Table 1). Elements that can be measured with precision include metacarpals I and III, manual phalanx I-1, manual unguals I and III, as well as pedal ungual III. Parts of the metacarpals Fig. 1 Overview of the “Haarlem specimen”, of Ostromia or their impressions are found on both the main and crassipes (Meyer, 1857). Counterslab, Teylers Museum TM 6929 (left) counterslab and can be used to establish the length of these and main slab, TM 6928 (right). Rectangles indicate areas detailed in elements. Thus, the proximal end of metacarpal I is Fig. 3 (yellow) and Fig. 6 (white) preserved on the main slab, whereas an impression of its distal end is present on the counterslab. The proximal part of metacarpal II is clearly preserved as impression on Archaeopteryx [12], and it has since been known as the the counterslab, but the distal end of this element is Haarlem specimen, as it is kept in Teylers Museum in obscured by a dissolved area, a typical feature of the lime- Haarlem, the Netherlands [13]. stones of Jachenhausen [17]. However, as the metacarpus A re-examination of the Haarlem specimen of Archaeop- was obviously preserved in complete articulation, the teryx failed to identify any shared apomorphic/diagnostic proximal end of metacarpal II is a good indicator for the characters with other Archaeopteryx specimens, but approximate position of the proximal end of metacarpal revealed important differences that make a referral to III, and most of the shaft and the distal end of the latter this taxon untenable, but indicate a relationship to are preserved as impression on the counterslab. Most of Anchiornis and relatives. manual phalanx I-1 is preserved on the counterslab, and both its proximal and distal extremities are clearly marked Methods Anatomical comparison Both the original of the Haarlem specimen, as well as a Table 1 Selected measurements of paravian theropods high quality cast kept at the Bayerische Staatssammlung Specimen mcI mcIII mpI-1 muI muIII tibia mt puIII für Paläontologie und Geologie in Munich were studied –– – –– 80.7 44.1 10.3 in detail, using binokular microscopes. The specimen 8.3 24.8 20.5 9.6 7.3 68.5 37 8.1 was compared to other specimens of Archaeopteryx on Maxberg 9.8 30 25 9.9 8.4 76.5 41.5 – the basis of personal observations of one or both of the Eichstätt 5.5 16.5 15.6 6.9 5.2 52.5 30.2 6.1 authors on all 12 known specimens of Archaeopteryx, Solnhofen –– 28 13.8 10.4 92 47.5 11.7 except the London and Maxberg specimens. However, of these specimens, high quality casts held at the BSPG München 7.2 23.5 20 9.2 6.7 73 40 7.4 were studied. Specimens of Anchiornis, including the Thermopolis 6.6 22 19.5 –– 74,6 39.6 – holotype, and several other theropods of the Jehol 11th 9.9 31.5 23.3 11.6 10 76.3 40.3 8.1 Biota were personally studied by one of us (CF), and Haarlem 10.5 23.2 23.1 9.5 8.3 80 48 7.8 high-resolution photographs of additional specimens of Anchiornis 12.5 30.5 26.2 15.6 13.8 106.4 55.2 13.7 Anchiornis, ,andAurornis were graciously Selected measurements (in mm) of the Haarlem specimen and several other provided by Markus Moser, Pei Rui, Helmut Tischlinger, specimens of Archaeopteryx, as well as the anchiornithid Anchiornis. and Wang Xiaoli. Measurements of the Haarlem specimen and measurements of unguals (except for Anchiornis) were taken by us, other measurements taken from The incomplete preservation of the Haarlem specimen Wellnhofer [13] and Hu et al. [32]. Abbreviations: mp, manual phalange; mc, (Fig. 1) precludes exact measurements for most long bones, metacarpal; mt, metatarsus; mu, manual ungual; pu, pedal ungual Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 3 of 16

as sharp impressions so that the length of this bone can in this specimen, so that this identification should be be established with certainty. Two manual unguals are regarded as tentative. preserved. One of them is associated, though not articu- lated with phalanx I-1 and is therefore interpreted as the Phylogenetic and paleogeographic analyses ungual of I. The other ungual is articulated with the In order to test the affinities of the Haarlem specimen, distal end of a slender phalanx distal to the dissolved area we added this specimen to an updated version of the on the counterslab. As the phalanx seems to be too slender phylogenetic matrix of Foth et al. [9]. Several character to represent the much more robust digit II, we concur with codings were revised, and one additional character was Ostrom [16] and Wellnhofer [13] that this element repre- added. Character coding for the OTU Archaeopteryx sents the ungual of digit III. The length of the unguals was was based on the pooled information from all specimens measured perpendicular to a line drawn through the dorsal that can be identified as belonging to a monophyletic and ventral extremity of the proximal articular end [18]. clade (here regarded as the genus Archaeotperyx, regardless Two pedal unguals and several impressions are present on of alternative generic names proposed for several speci- the main slab. One of these unguals can be measured mens and the still unresolved species ) based on precisely and is clearly associated with the impressions of thediagnosticcharactersproposedbyFothetal.[9]and the third digit of the right foot. additional unpublished information gathered by the The estimated elements are the tibiotarsus and meta- authors. Thus, for our analysis, this genus currently tarsus. As noted by Ostrom [16] and Wellnhofer [13], the includes the London, Berlin, Eichstätt, Solnhofen, Munich, preservation of the femora, tibia and fibulae, together with Daiting, Thermoplois, 11th, and 12th specimens, and, the position of the remains of the feet indicate that the most probably, also the Maxberg specimen. The resulting legs were preserved in complete articulation. Thus, data matrix thus contained 132 OTUs and 561 characters, although the distal end of the tibiotarsus and the proximal and is deposited on morphobank (www.morphobank.org) end of the metatarsus are missing, their approximate under project 2532. The matrix was analyzed using lengths can be estimated with a probably relatively small equally weighted parsimony in TNT [19] using a heuristic margin of error based on where these elements would search with 1000 replicates of Wagner trees followed by intersect. Our estimations are in accordance with those TBR branch swapping (holding 10 trees per replicate). given by Ostrom [16], but slightly higher than those pro- To evaluate node support 1000 bootstrap replicates were vided by Wellnhofer [13]. The reason for this seems to be calculated. that Wellnhofer seems to have measured the tibiotarsus of To establish the ancestral range of maniraptorans, we the right leg, which is slightly less flexed than the left leg used a Statistical Dispersal-Vicariance Analysis (S-DIVA) and thus displaced distally in respect to the latter, whereas [20], using the software RASP [21]. For the S-DIVA the impression of the metatarsus is of the left element. analysis, we ran a second phylogenetic analysis in TNT In order to statistically evaluate the significance of with only 100 replicates, to obtain a more manageable differences in proportions, we performed one sample t- and tree file. The analysis resulted in 190 equally parsimonious z-tests for the ratios of metacarpal III / metacarpal I, trees, the strict consensus of which is identical to that manual phalanx I-1 / metacarpal I, manual phalanx I-1 / recovered in the more extensive analysis described above. metacarpal III, manual ungual I / metacarpal I, manual These 190 trees were fed into RASP and used to calculate ungual III / metacarpal III and tibiotarsus / metatarsus, a condensed tree (=majority rule consensus) in this testing the Haarlem specimen against those specimens program for the biogeographic analysis. that can be classified as Archaeopteryx (or at least a One problem for biogeographic analyses based on such monophyletic ) based on the diagnosis a large dataset is the stratigraphic range of the taxa provided by Foth et al. [9]. The one sample tests compare covered [22]. Indeed, the phylogenetic matrix includes the value in question with the range of the comparative taxa ranging from the Middle Jurassic (: statistical population, in this case up to seven other speci- ) to Recent (several modern genera of birds) mens of Archaeopteryx, under the assumption of a normal and thus covers roughly 167 million years. This time span distribution, to evaluate the probability that this value saw profound changes in geography, with the Middle represents the same population, based on probability Jurassic representing the ultimate stages of the super- tables that account for sample size. Given the small continent Pangea, its initial break-up in the Late Jurassic sample size, the statistical power of these tests is rather and its fragmentation during the Cretaceous, up to the low. For the t- and z-tests, the values of the Maxberg configuration of the modern continents during the specimen have not been included; although the observ- Cenozoic. Thus, the current paleogeographical regions able morphology and proportions of this specimen are might have only limited value for analyzing biogeographic consistent with an identification as Archaeopteryx, none patterns at the time implicated for the major radiation of of the diagnostic characters of this taxon are preserved maniraptorans (Middle Jurassic). However, as the vast Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 4 of 16

majority of taxa come from a rather limited number of however, be seen with caution. Ostrom [16] and Wellnhofer relatively small regions, including eastern Asia (China and [13] noted the unusually long metatarsus in the Haarlem Mongolia), Europe, western North America, Madagascar, specimen as well, but as the distal end of the tibiotarsus and southern South America (Argentinean Patagonia), and the proximal end of the metatarsus are missing, they these areas can be used as proxies for the geographic speculated that this unusual measurement was due to a distribution of these over the entire time span. To displacement of the metatarsus from the ankle. However, as further test the influence of long time spans and thus also both knee joints are preserved in articulation, with hardly possible changes in the geographic distribution of taxa any space in between the and the tibia, there is no used as OTUs as opposed to their possibly much more reason to assume a displacement of the metatarsus by as antique ancestors, we reran two additional time-sliced much as 5 mm, the value needed to fall within the extremes analyses [22, 23], one with only Jurassic taxa and their of the range exhibited by the specimens that can securely interrelationships included, and one including Jurassic and be referred to Archaeopteryx. Thus, although the exact taxa. The second analysis was performed value might differ slightly, we tentatively regard this becauseJurassictaxaareactuallypoorlyrepresentedin difference in proportions as real. the data set, as few Jurassic coelurosaurs have been Both statistical tests rejected the null hypothesis that described so far (only 16 of 132 taxa of the complete the ratios for the Haarlem specimen were taken from the data set represent this time period, including the two same population as the ratios for the securely identified outgroup taxa). Archaeopteryx specimens at p < 0.002. In addition, the Haarlem specimens differs from Archaeopteryx in the Results ratio between the manual phalanx I-1 and metacarpal 1, Differences in proportions manual phalanx I-1 and metacarpal III and manual ungual Duetoitsincompleteness,noneofthediagnostic III and metacarpal III (Table 2). Although the statistical characters for the genus Archaeopteryx listed by Foth et power of the tests is low, given the low sample size, these al. [9] is preserved in the Haarlem specimen, so that a dir- differences indicate that there is little reason to refer this ect evaluation of the taxonomic referral is not possible. specimen to Archaeopteryx. However, the preserved elements show several differences to the corresponding parts of those specimens that can Osteological differences securely be referred to Archaeopteryx. Despite the limited Beside proportional differences, the Haarlem specimen data, several significant differences in proportions between shows a regular, well-developed longitudinal furrow on the Haarlem specimen and other specimens of Archaeop- the exposed medial side of the preserved manual phalanx teryx are obvious (Fig. 2; Table 2). Thus, the ratio between I-1 (Figs. 3b and 4). Although the margins of the phalanx the length of metacarpal III and metacarpal I (Fig. 2a) var- show signs of compression, the furrow itself is intact and ies between 2.99 (Berlin specimen) and 3.33 (Thermopolis does not show any signs of breakage due to collapse of the specimen) in Archaeopteryx, but is 2.21 in the Haarlem bone (Figs. 3b and 4). Furthermore, the impression of the specimen. Likewise, the ratio between manual ungual I lateral side of phalanx III-3 shows a very similar, regular and metacarpal I (Fig. 2b) varies between 1.16 (Berlin longitudinal ridge as counterpart to a furrow that was specimen) and 1.28 (Munich specimen) in Archaeopteryx, obviously present in this phalanx (Fig. 3b). The distal end but is 0.90 in the Haarlem specimen. A possible explan- of this phalanx is preserved as bone on the counterslab, ation for this difference could be that the ungual has been and also shows the distal end of such a furrow towards wrongly identified and might represent the ungual of digit the articular end of the medial side (Fig. 3b), indicating II or even of digit III of the left manus. However, ungual II that these furrows were present on both sides of the does not differ considerably in size from the ungual of manual phalanges; this is supported by the impression of the first digit in other specimens of Archaeopteryx [13], this phalanx on the main slab. A longitudinal furrow is and the difference in size between this ungual and the furthermore also present on the lateral side of a small preserved ungual of the right digit III, as well as the preserved fragment of metacarpal III (Fig. 3a), again with close association of this ungual with phalanx I-1 argue no indication of being caused by collapse of this element, against this interpretation. A further value in which the such as broken or irregular margins. None of the other Haarlem specimen differs significantly from other speci- specimens that can securely be identified as Archaeopteryx mens of Archaeopteryx is the length of the tibiotarsus in shows such regular furrows (e.g. Eichstätt, Munich, relation to the metatarsus (Fig. 2f), which varies between Thermopolis, and 11th specimens; CF and OR, pers. obs.; 1.74 (Eichstätt specimen) and 1.94 (Solnhofen specimen) Fig. 5a), although collapse structures are present in various in Archaeopteryx, but is 1.67 in the Haarlem specimen. As long bones of other specimens. In the Solnhofen specimen, the length of the tibiotarsus and metatarsus can only be for example, a longitudinal furrow seems to be present in estimated in the Haarlem specimen, this difference should, the basal part of the right phalanx I-1 and II-2, but these Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 5 of 16

Fig. 2 Scatterplots for several proportions that can be established in Ostromia (red dots), comparing this taxon with specimens that can certainly be referred to Archaeopteryx (black dots). Red line shows the ordinary least squares regression fit and blue lines represent the 95% confidence intervals for the distribution of values of Archaeopteryx. a Ratio between metacarpal III and metacarpal I. b Ratio between phalanx I-1 and metacarpal I. c Ratio between phalanx I-1 and metacarpal III. d Ratio between ungual I and metacarpal I. e Ratio between ungual III and metacarpal III. f Ration between metatarsal III and tibia Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 6 of 16

Table 2 Skeletal proportions in Archaeopteryx and Anchiornis grooves have irregular margins and show breaks at their mcIII/ mpI-1/ mpI-1/ muI/ muIII/ tibia/ deeper parts, indicating that they were caused by collapse mcI mcI mcIII mcI mcIII mt of the hollow bone (OR, pers. obs.; Fig. 5b). Indeed, the London –––––1.83 absence or, when present, very typical morphology of Berlin 2.99 2.47 0.83 1.16 0.29 1.85 such collapse structures in a wide variety of terrestrial Eichstätt 3.00 2.84 0.95 1.25 0.32 1.74 from the Solnhofen limestones, including lepidosaurs, crocoylomorphs, , and non-avialian Solnhofen –––––1.94 theropods, and their inconsistent appearance in various München 3.26 2.78 0.85 1.28 0.29 1.83 elements or only parts of elements in other Archaeopteryx Thermopolis 3.33 2.95 0.89 ––1.88 specimens differs drastically from the very regular 11th 3.18 2.35 0.74 1.17 0.32 1.89 structures found in all preserved manual phalanges in Anchiornis 2.46 2.11 0.86 1.22 0.45 1.93 the Haarlem specimen, thus supporting our interpretation Haarlem 2.21 2.20 1.00 0.90 0.36 1.67 that the regular furrows in the manual elements are primary structures in the latter. t-value 13.603 4.195 4.287 10.354 6.916 7.716 Further differences can be found in the , although p-value <0.001 <0.020 <0.020 <0.002 <0.01 <0.001 only parts of the distal shaft and the pubic boot of the z-value 6.083 1.876 1.917 5.179 3.458 2.916 right pubis are preserved on the main slab of the Haarlem p-value <0.001 0.038 0.024 <0.001 <0.001 0.001 specimen, while the shaft of the left pubis is indicated by Ratio of skeletal elements in the Haarlem and other Archaeopteryx specimens its impression (Fig. 6). Although the pubes were slightly (which can be diagnosed) and statistical differences (t-test and z-test) between compressed, and thus the shaft of the right pubis was the Haarlem specimen and Archaeopteryx. Abbreviations: mp, manual phalange; mc, metacarpal; mt, metatarsus; mu, manual ungual slightly displaced anteriorly in respect to that of the left

Fig. 3 Anatomical details of the manus of Ostromia crassipes and Anchiornis huxleyi. a Detail of the preserved elements of the right manus on the main slab, showing longitudinal furrows (or their impressions) in metacarpal III and the manual phalanges (arrows). b Detail of the preserved elements of the right manus on the counterslab of the holotype of Ostromia crassipes (TM 6929), showing longitudinal furrows (or their impressions) in the manual phalanges (arrows). c, d Impression (c) and high-resolution cast (d) of the left manus of the holotype of Anchiornis huxleyi (Institute of and Paleoanthropology IVPP V 14378), showing longitudinal furrows in the manual phalanges (arrows). All scale bars are 10 mm Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 7 of 16

Fig. 4 Details of manual phalanx I-1 of Ostromia crassipes, showing the regular development and non-collapsed margins of the longitudinal groove. a, stereophotograph. b, magnification of the shaft of the phalanx

pubis (as e.g. in the Solnhofen and Thermopolis speci- Having established significant differences between the mens), there is no indication of a break in the pubic shafts Haarlem specimen and those specimens that can securely in the rather clear impression, and the exposure of the be referred to Archaeopteryx, the fragmentary nature of pubic boot in lateral view indicates that the pubis was the former specimen make an identification of its affinities embedded mainly transversely in the sediment. Thus, the difficult. However, although the presence of longitudinal preserved parts of the pubis and the impression clearly furrows on the manual phalanges has not been described shows that the pubic shaft was strongly flexed, being in the literature, we found this character to be clearly anteriorly convex, in its medial part (Fig. 6). In those present in Anchiornis huxleyi, based on own observations Archaeopteryx specimens, where the pubis is exposed in by one of us (CF) on the holotype of this species (Institute lateral view (i.e. Berlin, Solnhofen, Munich, 11th, and 12th of and Paleoanthropology IVPP specimen) the bone is slender with a straight to very V14378). Although the only preserved manus in this spe- slightly curved shaft (Fig. 7b-d). Only the Thermopolis cimen is poorly preserved and has suffered from severe specimen seems to show a slightly flexed pubic shaft [24], breakage and erosion of the bones, the longitudinal fur- but the bone is seen in anterolateral view, making a final rows are clearly visible on the impression of the manus on validation impossible. In contrast, the curving in the pubic the counterslab (Fig. 3c, d). Despite generally poor bone shaft of the Eichstätt specimen is a preservational artefact, preservation in the specimens from the Tiaojishan Forma- caused by the right pubic apron, which was displaced tion, this observation could subsequently be confirmed in anteriorly during burial, forming a kink. However, the other specimens (STM0-52 [25]; XHPM 1084; CF pers. posterior margin of the pubic shaft is almost straight, as in obs.). Imprints of metacarpal III in the right manus of the other Archaeopteryx specimens, and the slight apparent STM0-52 indicates that the furrows were present on both flexure of the pubis shafts in these specimens still differs sides of the bone, as it is the case in Haarlem specimen considerably from the strongly flexed shafts in the Haarlem (see above). As in the case of the Haarlem specimen, the specimen. Furthermore, the pubic boot of the Haarlem spe- very regular appearance of these furrows in the specimens cimen is triangular in outline, with an almost straight distal we examined (Fig. 5e) argues against an interpretation as margin (Fig. 6), while in all other Archaeopteryx specimens, simple collapse structures. Similar furrows also seem to be where the shape of structure can be verified, the pubic boot present in the specimens described by Pei et al. ([26]: is distally convex and curves proximally posteriorly, resem- figs. 19, 28-30, although from the photos provided it is bling a the shape of a soup-ladle [9, 13] (Fig. 7b-d). impossible to determine with certainty whether these Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 8 of 16

Fig. 5 (See legend on next page.) Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 9 of 16

(See figure on previous page.) Fig. 5 Manual phalanges of several other theropods preserved in highly compacted sediments, showing differences (a-d, f) and similarities (e)in preservation to the manual furrows in the Haarlem specimen. a Right manus of the Thermopolis specimen of Archaeopteryx, showing non-collapsed phalanges without furrows, as they are found in many specimens of this taxon (e.g. London, Berlin, Eichstätt, Munich, 11th specimen). b Right manus of the Solnhofen specimen of Archaeopteryx, showing partially collapsed and crushed phalanges with clearly broken margins. c Left manus of albersdoerferi (BMMS BK 11) under UV light, showing partially compressed phalanges in this juvenile theropod. d Phalanx II-2 of longipes (SNSB-BSPG AS I 563), showing non-collapsed, but partially broken shaft. e Impression of phalanx I-1 of the holotype of Anchiornis huxleyi (IVPP V 14378), showing the impression of a regular longitudinal furrow, very similar to the impressions seen in the Haarlem specimen. f Phalanx I-1 of (IVPP V 12430), showing collapse structure distally with clearly broken margins. Scale bars are in mm increments structures might result from collapse of the phalanges. obs.) shows a weakly developed furrow on phalanx II-2 Furthermore, such furrows also seem to be present in the only, but it cannot be completely excluded that this manual phalanges of Eosinopteryx [27], but they are structure is due to collapse. However, these furrows are clearly absent in Xiaotingia [4]. Outside , a longitu- less well-developed than in the Haarlem specimen and dinal furrow can be found on phalanx I-1 (= phalanx II-1 do not occur on all manual phalanges or the metacarpals based on the terminology of Xu et al. [28]) of the basal (as with the presence of a groove on one phalanx only in troodontid Jianianhualong tengi (DLXH 1218 [28]). Less Jianianhualong). well-developed furrows are also present in at least some In addition, the Haarlem specimen resembles Anchiornis manual phalanges of the basal tyrannosauroids with respect to its pubis morphology. Although not (IVPP V14531; OR, pers. obs.) and (ZCDM preserved in the holotype [31], the specimens described V5001 [29]), and the paravians (IVPP by Hu et al. [32], specimen BMNHC PH822 described V9612; OR, pers. obs.) and (IVPP V12811 by Pei et al. ([26]: fig. 32), and specimens STM0-165, [30]). A specimen of Caudipteryx (IVPP V12430; CF, pers. STM0-52 [25] and STM-0-118 [33] show that the distal

Fig. 6 Pubic morphology of Ostromia. a Stereophotograph of the preserved pubis and impressions of the shaft, taken from a high quality cast at the BSPG. b outline reconstruction. Scale bar is 10 mm Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 10 of 16

Fig. 7 Comparison of pubic morphology of Ostromia (a)withArchaeopteryx (b-d)andAnchiornis (e, f). a Reconstructed pubis of Ostromia crassipes. b Pubis of the Berlin specimen of Archaeopteryx (photograph of high-quality cast at BSPG). c Pubes of the Munich specimen of Archaeopteryx.Note that the proximal shaft is of the left pubis, while the distal part is the right pubis, the proximal part of which is hidden by matrix. d Pubis of the11thspecimenofArchaeopteryx.Notethatpartoftheshaftoftherightpubisisvisible distally, creating the impression of a flexed shaft. However, any impression of these structures would clearly show two pubic shafts, unlike the situation in the Haarlemspecimen(seeFig.5a). e Pubis of Anchiornis (BMNHC PH822; photo courtesy Rui Pei). f Pubis of Anchiornis (STM0-165; photo courtesy Wang Xiaoli) two thirds of the pubic shafts in this taxon are strongly taxon on this material. However, a species name for this flexed, and that the pubic boot has a similar, triangular specimen already exists, as it was originally named as a outline (Fig. 7e, f). new species of the pterosaur Pterodactylus, P. crassipes, by von Meyer [11]. Thus, in order to conserve this name, Phylogenetic and taxonomic status of the Haarlem specimen and as the specimen cannot be referred to any known The parsimony analysis retained more than 15.580 equally genus, we propose a new generic name for P. crassipes. parsimonious trees with a length of 2624 steps. The strict Like our analysis, previous studies have found Anchiornis consensus tree shows a reasonably good resolution and to form a clade with Xiaotingia (e.g [4, 8–10, 33, 34]), but largely conforms to the tree published by Foth et al. [9] also Eosinopteryx [10, 26]. As outlined above, the available (see Additional file 1). The Haarlem specimen did not character evidence also place the Haarlem specimen in this cluster with Archaeopteryx, but was found in a polytomy lineage. Based on this topology, and given that this clade together with , Eosinopteryx,andAnchiornis,to represents an important taxon within the plexus of derived the exclusion of Xiaotingia, which represents the sister maniraptorans surrounding the evolutionary origin of avia- taxon to this polytomy (Fig. 9). The bootstrap values of lans, we propose a new clade, named Anchiornithidae. the phylogeny are generally low, and only two additional steps are needed to move the specimen as sister taxon to Systematic Palaeontology Archaeopteryx. However, as only 46 characters could be coded for the Haarlem specimen, and most of these are Marsh, 1881 [35] plesiomorphies at the node of Avialae, two additional steps Maniraptora Gauthier, 1986 [36] actually represent a rather large part of the character Anchiornithidae tax. Nov. transformations that help placing this taxon. genus. Anchiornis Xu, Zhao, Norell, Sullivan, Apart from the fact that there are no anatomical charac- Hone, Erickson, Wang, Han, and Gao, 2009 [31]. ters that unambiguously support a referral to Archaeopteryx, Definition. Anchiornithidae is a stem-based taxon the results of the phylogenetic analysis thus support the re- defined as all maniraptoran theropods that are more closely moval of the Haarlem specimen from this genus. Given the related to Anchiornis huxleyi than to Passer domesticus, very incomplete and rather poor preservation of the Archaeopteryx lithographica, albertensis, specimen, the question arises whether to base a new formosus,orOviraptor philoceratops. Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 11 of 16

Diagnosis. Based on the evaluation of character trans- phalanges and at least metacarpal III. The taxon differs formations in the phylogenetic hypothesis presented here, from other anchiornithids in an unusually small first the following morphological characters can currently be manual ungual and other proportions. Measurements used to diagnose Anchiornithidae: Nutrient foramina on for an almost complete specimen of Anchiornis were dentary placed in deep groove (convergently present in given by Hu et al. [32], and this specimen differs from most troodontids and some other coelurosaurs); anterior Ostromia in the relative length of metacarpal III in dentary teeth smaller, more numerous, and more closely comparison to metacarpal I (2.46 versus 2.21), the appressed than those in the middle of the row length of the first manual ungual in comparison to meta- (convergently present in most troodontids); anterior carpal I (1.26 versus 0.9), and the length of the tibiotarsus in edge of acromion margin of laterally everted or comparison to the metatarsus (1.93 versus 1.67) (Table 2). hooked (convergently present in several oviraptorosaurs In contrast, only a few selected measurements were given and more derived avialans); medial surface of proximal for Eosinopteryx [27], so that the only comparable ratio is fibula flat (convergently present in alvarezsaurids, therizino- that between the tibiotarsus and the metatarsus, which is sauroids and derived avialans); fan-shaped posterior dorsal 1.96 in Eosinopteryx, as opposed to 1.67 in Ostromia.Fur- neural spines (convergently present in compsognathids and thermore, although no measurements are given, the some derived avialans); extensive large pennaceous photo of the manus of Eosinopteryx clearly shows that on metatarsus and pes (convergently present in manual ungual I is longer than metacarpal I in this taxon, and ). rather than shorter, as it is the case in Ostromia. Further possible diagnostic characters include the Apart from the geographic and stratigraphic differences following: Retroarticular process of the mandible curves (Anchiornis and Eosinopteryx are of Oxfordian age, whereas posterodorsally (only known in Xiaotingia; convergently Ostromia comes from the early ; Schweigert, present in derived ornithomimosaurs and aves); shallow pers. com.), these differences indicate that the European Meckelian groove in dentary (only known in Xiaotingia; anchiornithid is different from its Chinese cousins so that convergently present in several tyrannosauroids and derived the proposal of a new generic name seems justified. A full avialans); presence of a posterior flange on manual phalanx anatomical description of this specimen was provided by II-1 (only known in Anchiornis;convergentlypresentin Ostrom [16]. some dromaeosaurids and advanced avialans); presence of a shelf-like supraacetabular crest of (currently Discussion only known in Anchiornis; reversal to the basal tetanuran Ostromia as a separate genus condition, convergently present in alvarezsaurids and In his detailed description of the Haarlem specimen, several avialans); anteriorly convex pubic shafts (present in Ostrom [16] noted several possible differences in propor- Anchiornis and the Haarlem specimen, apparently absent tion between this and other specimens of Archaeopteryx in Eosinopteryx; convergently present in some dromaeo- then known, most notably in the relative length of the saurids and more derived avialans). metatarsus and the manual unguals. However, he assigned these differences either to preservational artifacts (in Ostromia gen. nov. the case of the metatarsus) or individual variation. The re-exanimation of the Haarlem specimen in combin- Etymology. The generic name honours the late John ation with a broad-scale phylogenetic analysis did not Ostrom, who identified the Haarlem specimen as a theropod. find any shared unique characters of this specimen with the genus Archaeopteryx, but highlighted several propor- Ostromia crassipes von Meyer, 1857 [11] tional and anatomical differences and thus strongly implies that this specimen is not an Archaeopteryx, but represents Holotype. Teylers Museum TM 6928, 6929, part and a different genus and species, Ostromia crassipes,whichis counterpart of a fragmentary skeleton. closely related to the basal avialan Anchiornis from the Locality and horizon. Jachenhausen locality, near lower Upper Jurassic of China. Riedenburg, Bavaria, Germany. Early Tithonian laminated Although the differences in proportions are statistically limestones of the Painten Formation [37]. significant, it must be noted that the statistical power of Diagnosis. Due to the poor preservation of the holotype, the statistical tests performed is low, given the very low this species cannot be distinguished from other theropods sample size. However, these results support the notion strictly on apomorphic characters; only a differential that the specimen is significantly different from Archae- diagnosis can be given. Ostromia crassipes differs from opteryx. More importantly, in the absence of any discrete most theropods with the probable exception of Anchiornis anatomical characters that would support a referral of and Eosinopteryx (as closest relatives) in the presence of the Haarlem specimen to Archaeopteryx, and the general longitudinal furrows on both sides of all preserved manual anatomical similarity of many basal paravian theropods, Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 12 of 16

these differences in basically all of the few comparable theropods in general. All described skeletal specimens of proportions are a strong indication that this specimen Archaeopteryx come from the Solnhofen, Eichstätt and should be removed from that genus. Daiting area [13], with the exception of the so far unde- The nature of the osteological features that distinguish scribed 12th specimen, which comes from Schamhaupten the Haarlem specimen from Archaeopteryx could be [39], some 30 km to the east (Fig. 8). Ostromia comes from questioned on the basis of the incompleteness of the the locality of Jachenhausen [13], 10 km further to the specimen and strong taphonomic compaction. Although north-east from Schamhaupten. The Jachenhausen locality the reconstruction of the pubis, for instance, is partly is at the westernmost rim of the Painten Basin, one of the based on imprints in the matrix, we interpret the shape to easternmost plattenkalk basins within the Solnhofen archi- be reliable, based on the general quality of the imprints, as pelago. These eastern basins (Schamhaupten, Painten, seen in other parts of the skeleton, such as the manual Hienheim, Kelheim, and Brunn basins) seem to have a and pedal phalanges. Furthermore, as the preserved higher terrestrial influence than the western basins, as remains indicate that the specimen was embedded lying indicated by abundant plant remains, lepidosaurs, and the on its side, there is no reason to assume that compression non-avian theropod dinosaurs Compsognathus, Juravena- would affect the anteroposterior flexure of the pubic shafts tor,andSciurumimus [40–43] (Fig. 8). The identification and the shape of the pubic boot, both of which are pre- of Ostromia as an anchiornithid adds to this remarkable served in lateral view. diversity of theropods in these eastern areas, and under- As noted above, the phalanges themselves show no signs lines the faunal differences with the western occurrences, of collapse due to compression, so that the longitudinal for which Archaeopteryx remains the only theropod furrows are interpreted to be real structures. As with most recorded, although in greater abundance than the different long bones of coelurosaurian theropods, manual phalanges taxa in the eastern basins. Apart from a slight stratigraphic are usually thin-walled and hollow. Especially in specimens difference between some of the eastern and western from strongly compressed sediments, such as the litho- plattenkalks, this most likely reflects different settings in graphic limestones of southern Germany and Las Hoyas these areas: whereas terrestrial organisms in the eastern (Spain) or the lacustrine deposits of the Daohugou and area might have come directly from the larger land mass Jehol beds, this might lead to a collapse of these bones, of the Bohemian massif to the east or from islands within resulting in often crushed elements that might show the directly adjacent coral reef zone [44], the western unnatural depressions or indentations (see e.g. Fig. 5b–f). occurrences were considerably more remote from any As noted above, however, the collapse structures in the larger land mass, and terrestrial animals might only come phalanges and other long bones of other Archaeopteryx from isolated small islands [42]. In this setting, even very specimens from the laminated limestones of southern limited flight capabilities might have represented a crucial Germany differ considerably from the very regular furrows advantage for a taxon like Archaeopteryx to invade these found in the Haarlem specimen (Figs. 4 and 5). Various more remote habitats. Thus, the occurrence of this taxon basal birds from the Jehol group show a combination of in a more marine setting represents indirect further longitudinal furrows and multiple, irregular breakages evidence for at least some sort of flight capabilities in of phalanges and metacarpals, while in many other Archaeopteryx. specimens these bones stay intact (extensively figured in Chiappe and Meng [38]). Although the holotype and The radiation and dispersal of maniraptoran theropods various referred specimens of Anchiornis show severe Apart from its significance for our understanding of the cases of breakage and erosion in the skeleton, including fauna of the Solnhofen archipelago, the identification of the forelimbs, we interpret the repeatable presence of Ostromia as an anchiornithid represents an enormous longitudinal furrows along the main axis in the manual range extension for this paravian clade from the Tiaojishan phalanges in multiple specimens of Anchiornis to be a real Formtaion of China to central Europe. All three S-DIVA structure and not an artefact of compression. This is analyses (with the entire data set and the two time-sliced supported by our own observations of several specimens, sets) indicate that, whereas there is no clear biogeographic including the holotype (IVPP V14378), in which these fur- signal for the origin and initial diversification of coelur- rows (or their natural molds) are more regular than would osaurs, the radiation of maniraptoran theropods more be expected for collapse structures (Figs. 3c, d and 5e). derived than the basal taxon , including Alvarezsauroidea, , /Eumaniraptora, Theropods in the Solnhofen archipelago , and Avialae, most likely happened in eastern The result of our re-evaluation of the Haarlem specimen Asia, as all nodes leading to the major clades within has far-reaching consequences for our understanding of Maniraptora are optimized for this area (Fig. 9; see the theropod fauna of the Solnhofen Archipelago, but also Additional file 1). Alternative phylogenetic positions like for the early evolution and biogeography of maniraptoran that for the aberrant theropod (basal Avialae Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 13 of 16

Fig. 8 Occurrence of Ostromia within the “Solnhofen Archipelago” and distribution of theropod dinosaurs in the Jurassic of that area. Modified from Butzmann et al. [72]

([45, 46]; this study) vs. basal Paraves [5, 27, 34, 47] vs. Cretaceous. This scenario is supported by another recent basal Oviraptorosauria [8, 10] or Anchiornis (basal Deino- analysis of dinosaurian biogeography [56], which found a nychosauria [4, 34] vs. basal Troodontidae [32, 47] vs. basal peak in connectivity between the continents in the Late Avialae ([8, 31], this study) would not change the outcome Jurassic, indicating that Europe was a “turntable” for of the analyses. dispersal during that time. In this scenario, the occurrences of an anchiornithid and Although this rapid, eastern Asian radiation of advanced Archaeopteryx in the Solnhofen Archipelago represent two maniraptorans is our preferred hypothesis in the light of phylogenetically (although not necessarily temporally) dis- the currently available evidence, it should be noted that it tinct dispersal events from eastern Asia to central Europe cannot be excluded that this might, at least partially, be an in the Late Jurassic. Given the probably Oxfordian age artifact of the fossil record. Prior to the recent description of the anchiornithids from the Tiaojishan Formation of abundant maniraptoran theropods from the Oxfordian [6], basically all maniraptoran clades must have been of China ([4, 5, 27, 31, 34, 45, 46, 57, 58]), no certain pre- established by this time, including the lineage leading to representatives of this clade were known. Archaeopteryx and higher avialans [48]. On the other hand, Late Middle Jurassic small theropod remains are exceed- the oldest certain records of coelurosaurs are Bathonian ingly rare globally, but a few specimens, mainly isolated in age and come from Europe [49] and central Asia teeth, have been referred to paravian clades, most notably [50]. As eastern Asia seems to have been isolated from dromaeosaurids (e.g. [59–61]). However, teeth similar to the rest of Laurasia by epicontinental seas by the those found in dromaeosaurids are also present in basal at the latest [51], the biogeographic pattern, together with tyrannosauroids ([49]) and, probably, the juvenile dentition the stratigraphic occurrences of taxa and palaeogeographic of more basal theropods ([40]), so more conclusive remains reconstructions indicate a rapid, seemingly explosive would be needed to prove the existence of pre-Late Jurassic radiation of maniraptoran theropods in isolation in eastern paravians in areas outside eastern Asia. Likewise, most pos- Asia in the late Middle Jurassic (Bathonian-Callovian), sible maniraptoran remains from Late Jurassic extra-Asian with a subsequent dispersal from eastern Asia towards localities are fragmentary (e.g. [62–64]) and rather incon- Europe and North America, in the Late Jurassic (Fig. 9), clusive. Even if confirmed, the presence of maniraptoran and further radiations and dispersals to South America theropods in the Kimmeridgian-Tithonian of Europe or the [52, 53], Madagascar [54] and Africa [55] during the Morrison Formation would not contradict the hypothesis Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 14 of 16

Fig. 9 Time calibrated simplified phylogeny of maniraptoran theropods, indicating place of origin of the different clades. The relationships and stratigraphic and geographic distribution of maniraptorans indicate a rapid radiation in the late Middle to earliest Late Jurassic in eastern Asia. Node labels and abbreviations: 1, ; 2, ; 3, Maniraptora; 4, ; 5, Paraves; 6, Avialae; BAJ, ; , Bathonian; BER, Berriasian; CAL, Callovian; KIM, Kimmeridgian; OXF, Oxfordian; TIT, Tithonian. Based on a phylogenetic analysis of 2 outgroups and 130 coelurosaurian ingroup taxa and 561 characters and the results of a S-DIVA analysis presented here, as they might result from a rapid Late in the Cenozoic [70]. As exemplified by Archaeop- Jurassic dispersal of this group over the Laurasian teryx, flight ability might have further increased the continents. dispersal potential for paravians, in which some form However this may be, the biogeographic pattern of flight capacity most probably evolved more than presented above might furthermore be mirrored by once [9, 34]. goniopholid crocodiles [65] and some pterosaur clades [66], which also seem to have expanded their range from eastern Asia towards Europe in the Late Jurassic. Conclusions Palaeogeographic reconstructions indicate that at least A re-evaluation of one of the twelve skeletal specimens a narrow marine barrier, probably with numerous islands, referred to the ‘Urvogel’ Archaeopteryx, the Haarlem existed between Asia and Europe up to the Tithonian, when specimen, revealed that this specimen represents a these landmasses might have been joined [67]. Whereas for separate taxon, Ostromia crassipes. Phylogenetic analysis crocodiles, different tolerances to brackish or even marine identifies Ostromia as the first representative of the basal waters were evoked to explain the ability to cross the still avialian clade Anchiornithidae outside eastern Asia. In remaining marine barrier through island hopping [65], combination with a biogeographic analysis, a rapid radi- flight ability was probably the key factor in the biogeo- ation of maniraptoran theropods in eastern Asia with a graphical evolution of pterosaurs [66]. For maniraptorans, subsequent dispersal of many lineages in the Late Jurassic small body size of the taxa at the base of all major lineages is indicated; dispersal of maniraptorans was facilitated by [68] might have made oversea dispersal by rafting possible small body size of basal members of all clades and, [69], thus facilitating the crossing of the epicontinental possibly, several independent acquisitions of flight cap- barriers between Asia and Europe. abilities. In the fragmenting world of Pangean break-up TheseparateAsianoriginofthelineagesofOstro- during the Late Jurassic and Cretaceous, increased mia and Archaeopteryx implied by the biogeographic dispersal potential might have been a key factor to analysis indicates that this dispersal might have hap- explain the success of maniraptoran, and especially pened in several independent waves, as has recently avialian theropods, with dispersal events being followed by been suggested for the evolution of oscine endemic radiations of different clades [71]. Foth and Rauhut BMC Evolutionary Biology (2017) 17:236 Page 15 of 16

Additional file Received: 10 May 2017 Accepted: 16 November 2017

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